TY - JOUR
T1 - Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas
JF - Proceedings of the National Academy of Sciences
JO - Proc Natl Acad Sci USA
SP - E226
LP - E235
DO - 10.1073/pnas.1712321115
VL - 115
IS - 2
AU - Łukasik, Piotr
AU - Nazario, Katherine
AU - Van Leuven, James T.
AU - Campbell, Matthew A.
AU - Meyer, Mariah
AU - Michalik, Anna
AU - Pessacq, Pablo
AU - Simon, Chris
AU - Veloso, Claudio
AU - McCutcheon, John P.
Y1 - 2018/01/09
UR - http://www.pnas.org/content/115/2/E226.abstract
N2 - Highly reduced genomes from bacteria that are long-term beneficial endosymbionts of insects often show remarkable structural stability. Endosymbionts in insects diverged by tens or hundreds of millions of years often have genomes almost completely conserved in gene order and content. Here, we show that an endosymbiont in some cicadas has repeatedly and independently fractured into complexes of distinct genomic and cellular lineages present in the same host. Individual endosymbiont lineages, having lost many of the essential ancestral genes, rely on each other for basic function and together seem to provide the same nutritional benefits as the ancestral single symbiont. These cicada endosymbionts show genomic parallels to mitochondria and provide another example of how normally stable genomes can lose structural stability.Bacterial endosymbionts that provide nutrients to hosts often have genomes that are extremely stable in structure and gene content. In contrast, the genome of the endosymbiont Hodgkinia cicadicola has fractured into multiple distinct lineages in some species of the cicada genus Tettigades. To better understand the frequency, timing, and outcomes of Hodgkinia lineage splitting throughout this cicada genus, we sampled cicadas over three field seasons in Chile and performed genomics and microscopy on representative samples. We found that a single ancestral Hodgkinia lineage has split at least six independent times in Tettigades over the last 4 million years, resulting in complexes of between two and six distinct Hodgkinia lineages per host. Individual genomes in these symbiotic complexes differ dramatically in relative abundance, genome size, organization, and gene content. Each Hodgkinia lineage retains a small set of core genes involved in genetic information processing, but the high level of gene loss experienced by all genomes suggests that extensive sharing of gene products among symbiont cells must occur. In total, Hodgkinia complexes that consist of multiple lineages encode nearly complete sets of genes present on the ancestral single lineage and presumably perform the same functions as symbionts that have not undergone splitting. However, differences in the timing of the splits, along with dissimilar gene loss patterns on the resulting genomes, have led to very different outcomes of lineage splitting in extant cicadas.
ER -